Controls on soil respiration in semiarid soils

Richard T. Conanta,*, Peter Dalla-Bettab, Carole C. Klopatekc, Jeffrey M. Klopatekd

aNatural Resource Ecology Laboratory, Colorado State University, 131 East Drive, Fort Collins, CO 80523-1499, USAbDepartment of Geology, Arizona State University, Tempe, AZ 85287-1404, USA

cUSDA Forest Service, Arizona State University, Tempe, AZ 85287-2701, USAdDepartment of Plant Biology, Arizona State University, Tempe, AZ 85287-1601, USA

Received 28 April 2003; received in revised form 21 January 2004; accepted 27 February 2004

Abstract

Soil respiration in semiarid ecosystems responds positively to temperature, but temperature is just one of many factors controlling soil

respiration. Soil moisture can have an overriding influence, particularly during the dry/warm portions of the year. The purpose of this project

was to evaluate the influence of soil moisture on the relationship between temperature and soil respiration. Soil samples collected from a

range of sites arrayed across a climatic gradient were incubated under varying temperature and moisture conditions. Additionally, we

evaluated the impact of substrate quality on short-term soil respiration responses by carrying out substrate-induced respiration assessments

for each soil at nine different temperatures. Within all soil moisture regimes, respiration rates always increased with increase in temperature.

For a given temperature, soil respiration increased by half (on average) across moisture regimes; Q10 values declined with soil moisture from

3.2 (at 20.03 MPa) to 2.1 (21.5 MPa). In summary, soil respiration was generally directly related to temperature, but responses were

ameliorated with decrease in soil moisture.

q 2004 Elsevier Ltd. All rights reserved.

Keywords: Soil respiration; Soil carbon; Litter quality; Soil moisture; Pinyon–juniper; Ponderosa pine; Desert scrub

1. Introduction

Global soil respiration is estimated to be 76.5 pg C per

year which is 30–60 pg C per year greater than global net

primary production (Raich and Potter, 1995) and is thus a

very substantial flux in the global C cycle (Schimel, 1995).

Reviews of laboratory-based soil respiration measurements

have found that the soil respiration increases

with temperature. Rates of response, quantified using a

Q10 relationship, are inversely related to temperature

(Kirschbaum, 1995; Lloyd and Taylor, 1994): soils from

colder climates are more sensitive to increases in tempera-

ture. This relationship between soil respiration and tem-

perature has been successfully incorporated into a number

of soil organic matter models (e.g. Century and Roth C,

Jenkinson and Rayner, 1977; Parton et al., 1987). While

some aspects of temperature controls on soil respiration

have recently been questioned (Giardina and Ryan, 2000;

Holland et al., 2000), it is clear that soil respiration responds

positively to temperature in a number of systems and that

temperature is just one of a host of variables that influences

soil respiration (Davidson et al., 2000).

Field-based soil respiration measurements demonstrate

that Q10 values for soil respiration can vary spatially

(Conant et al., 1998) and seasonally (Borken et al., 1999;

Davidson et al., 2000) and are related to the distribution of

soil moisture. Soil moisture can influence soil respiration for

all or part of the year particularly in arid or semiarid

ecosystems (Amundson et al., 1989; Conant et al., 2001),

but also in more mesic systems (Borken et al., 1999;

Davidson et al., 1998; Gardenas, 2000; Savage and

Davidson, 2001). Soil moisture can limit soil respiration

by limiting microbial contact with available substrate and

dormancy and/or death of microorganisms at low soil water

potentials (Orchard and Cook, 1983). Arid and semiarid

lands (areas where precipitation exceeds annual potential

evapotranspiration) comprise more than one-third of the

earth’s surface (Koppen, 1954) and it is likely that

temperature-driven increases in soil respiration are

dampened by low soil moisture for part or all of the year

in these areas (Raich and Potter, 1995). The purpose of this

0038-0717/$ - see front matter q 2004 Elsevier Ltd. All rights reserved.

doi:10.1016/j.soilbio.2004.02.013

Soil Biology & Biochemistry 36 (2004) 945–951

www.elsevier.com/locate/soilbio

* Corresponding author. Tel.: þ1-970-491-1919; fax: þ1-970-491-1965.

E-mail address: conant@nrel.colostate.edu (R.T. Conant).

work was to evaluate the influence of soil moisture on the

relationship between temperature and short-term micro-

bially-mediated soil respiration rates. Soils from a series of

semiarid sites, situated along an elevation gradient, with

different soil C contents, vegetative communities, microbial

communities (i.e. fungal vs. bacterial populations), mean

annual temperatures, and mean annual precipitation were

incubated under a range of independently varying

temperature and moisture conditions. The interplay of

these four controlling factors (temperature, moisture,

microbial community structure, and soil C) were evaluated

in order to better understand (1) moisture-driven limits to

the positive relationship between temperature and soil

respiration and (2) variability of respiration responses to

increased temperature across a range of temperatures.

2. Materials and methods

The research area is located in the Coconino National

forest, due north of Flagstaff, Arizona on the leeward side of

the San Francisco mountains between 358250N, 1118340W

and 358260N, 1118400W. The area covers a 7 km transition

zone with great basin desert scrub (DS) at the lower

elevation, pinyon–juniper woodlands (PJ) in the middle,

and ponderosa pine (PP) forest at the upper elevation.

The DS site is dominated by winterfat (Ceratoides lanata

(Pursh) Moq.), snakeweed (Gutierrezia sarothrea (Pursh)

Britt. and Rusby), rubber rabbit brush (Chrysothamnus

nauseosus (Pall.) Britton.) and blue grama grass (Bouteloua

gracilis (H.B.K.) Lag.). The PJ site contains one-seed

juniper (Juniperus monosperma (Engelm.) Sarg.) and

pinyon pine (Pinus edulis Engelm.), with blue grama

dominant in interspaces. The PP site is an open, park-like

stand of PP (Pinus ponderosa Doug. ex Laws.) with mutton

grass (Poa fendleriana (Steud.) Vasey), mountain muhly

(Muhlenbergia montana (Nutt.) Hitchc.) and buck brush

(Ceanothus fendleri Gray.) in the understory.

Soils at all sites were derived from volcanic material and

are classified as Typic Haplustolls at the DS site grading into

Aridic Argiustolls at the PJ site and Typic Argiborolls at the

PP site. Soils are all sandy loams and are basic (pH ¼ 7.5) to

slightly acidic (pH ¼ 6.6). Mean annual temperatures based

on 30 years of climatic data range from 8.5 8C at the DS site

to 5.5 8C at the PP site and mean annual precipitation ranges

from approximately 320 mm per year at the DS site to

530 mm per year at the PP site (Klopatek et al., 1998)

(Table 1).

Four replicate mineral soil samples, consisting of surface

(0–15 cm) composites from six locations, were collected in

early march (just after snowmelt) from randomly located

interspace locations at each of the three sites and from

underneath four randomly selected canopies of each tree

type (pinyon and juniper canopies at the PJ site; PP canopies

at the PP site). Samples were sealed in plastic bags, returned

to the lab at field moisture, and stored under refrigeration

(4 8C). Samples were passed through a 2 mm sieve to

remove rocks and coarse roots; finer roots were then hand

picked from each sample. Gravimetric soil moisture was

determined on a 20 g subsample by oven drying at 70 8C for

24 h. Soil pH was measured in a 1:1 soil to 0.01 M CaCl2solution. Soil texture, was determined using the hydrometer

method and soil C and N contents were determined on a

Perkin–Elmer 2400 CHN Autoanalyzer (Perkin–Elmer,

St Joseph, MO).

Water potential was determined on all soil samples using

a pressure plate apparatus. Soil samples (25 g) contained in

metal rings with fine mesh bases were wet to field capacity

and exposed to increased atmospheric pressure.

Samples were allowed to equilibrate for 24 h at each

pressure increment (20.03, 20.50, 21.00, and

21.50 MPa) and were then weighed to determine water

holding capacity at each pressure. Sterile nanopure water

was injected into the soil samples to bring them to the proper

soil moisture. If soil moisture content was greater than soil

water content desired for incubations, the soil was air dried

for 24 h and sterile nanopure water was added back to the

soil to establish the proper soil moisture content (Table 2).

Bulk soil incubations were performed using 50 g of each

replicate soil sample in 500 ml sealed glass jars topped with

rubber septa. Soils were incubated at four temperatures

(5, 15, 15, and 35 8C) maintained by water baths and

constant temperature chambers, and four water holding

capacities (20.03, 20.50, 21.00, and 21.50 MPa). Head-

space CO2 concentration was determined initially and after

5 days of incubation by collecting a 100 ml sample of

headspace gas from each jar using a 500 l gas-tight, locking

syringe (Hamilton, Reno Nevada) and analyzed using a gas

chromatograph. CO2 concentration of headspace gas

samples was determined using a Perkin–Elmer Sigma

2000 gas chromatograph with a thermal conductivity

detector fitted with an Alltech 6 ft £ 1/8 in. stainless steel

80/100 mesh Poropak Q column. Nitrogen was the carrier

gas at 30 ml min21. The injector, detector, and column were

set at 150, 225, and 50 8C, respectively. A jar without soil

served as a CO2 blank. Soil respiration was assumed to

equal the change in CO2 concentration over the

incubation period minus the changes in concentration in

the blanks.

Table 1

Site characteristics for the three sites from which soils were collected for

this experiment from Klopatek et al. (1998)

Site Mean annual

temperature (8C)

Mean annual

precipitation (mm)

Elevation

(m)

Desert scrub

(DS)

8.5 310 1987

Pinyon–juniper

(PJ)

7.1 410 2126

Ponderosa pine

(PP)

5.5 530 2295

R.T. Conant et al. / Soil Biology & Biochemistry 36 (2004) 945–951946

Substrate-induced (SI) respiration rates were performed

to evaluate impacts of substrate quality on short-term soil

respiration responses to temperature. Three replicate soil

samples (2.5 g wet wt.) were added to 40 ml vials sealed

with teflon-lined silicon septa. Sterile nanopure water was

added to give a final ratio of 2:1 on a dry weight basis. Filter

sterilized (0.2 mM) D-glucose was then added from a 1 M

stock solution to give a final concentration of 20 mg ml21;

0.5 mg was added to each gram of soil. This concentration

demonstrated to saturate respiratory activity in these soils

within the time frame of these experiments. The vials were

then laid horizontally in a reciprocating water bath

(180 rpm) and incubated at the respective temperatures

(4, 10, 15, 20, 26, 30, 35, 40, and 45 8C) for 30 min at which

time 100 ml of the headspace was sampled and injected into

the gas chromatograph. A second sample was taken 1–2 h

later to determine the respiration rate. Optimization

experiments demonstrated that the rate of CO2 evolution

was linear in this time frame.

All analyses were carried out on field replicates.

Differences between incubation temperatures and moistures

were compared statistically using one-way analysis

of variance and Scheffe’s means comparison test in SAS

(SAS, 1985). Soil respiration quotients (Q10s) for bulk soil

incubations and SIR incubations were determined by

dividing the difference in soil respiration rates for two

incubation temperatures by the difference in incubation

temperature. Reported Q10 values are averages across all

(positive) increments.

3. Results

Soil respiration rates for DS soils ranged from 2.9 to

61.4 mg CO2 – C mg soil C21 d21. Within all water

potentials, respiration rates always increased with increase

in temperature (Fig. 1). Soil respiration rates under the

warmest incubation temperatures averaged four fold more

than those under the driest conditions; the largest difference

(nearly eight fold) occurred in the wettest soil (Fig. 1).

Across all incubation temperatures soil respiration increased

to an average of 72% between moisture classes.

Table 2

Soil texture and soil moisture at field capacity for the six soils used in this experiment

Soil Cover

type

Sand (%) Silt (%) Clay (%) Water holding capacity

(g H2O g soil21)

Soil C

(kg C ha21)

C:N

DS-I Interspace 70.7 15.6 13.7 0.16 10.5 10.5

PJ-I Interspace 63.7 13.6 22.7 0.22 11.9 9.2

PJ-J Juniper canopy 72.6 13.6 13.8 0.16 17.9 12.8

PJ-P Pinyon canopy 66.1 12.6 21.3 0.17 15.8 11.3

PP-I Interspace 69.7 12.3 20.0 0.14 12.3 17.6

PP-PP Ponderosa pine canopy 69.7 12.7 17.6 0.21 16.2 20.3

Soil names refer to the site and cover type of origin.

Fig. 1. Soil respiration for soils from the desert scrub (DS) site incubated under four temperatures and four soil moisture contents. Different lower case letters

indicate significant ðP , 0:05Þ differences between samples incubated under similar temperatures but different soil moisture contents. Different capital letter

indicate significant ðP , 0:05Þ differences between samples incubated under similar soil moistures, but different temperatures.

R.T. Conant et al. / Soil Biology & Biochemistry 36 (2004) 945–951 947

Soil respiration rates were significantly ðP , 0:05Þ greater

in the wetter soils (20.03 and 20.50 MPa) than in the two

driest soils with the exception of the difference between the

soils incubated under 20.03 and 20.50 MPa at 5 and 15 8C

(Fig. 1). On average, soil respiration was 2.5 times greater

under the wettest incubation conditions than under the driest

conditions and increased to an average of 50% across all

one-step moisture increases. Soil respiration rates

decreased with decreasing water potential with all incu-

bation temperatures (Fig. 1).

Responses to different incubation temperatures and

moisture contents at the PJ site were similar to those at

the DS site (Fig. 2). The range of soil respiration

rates observed for interspace soils collected from the PJ

site (5.6–47.8 mg CO2–C mg soil C21 d21) was narrower

than that observed at the DS site. Rates for soils collected

under canopies at the PJ site averaged 80% greater than

those from interspaces across all treatments. Soil respiration

rates for soils collected under canopies ranged from 6.1 to

135.0 mg CO2–C mg soil C21 d21. Soil respiration rates

tended to be greatest at the 25 8C incubation temperature.

The difference in soil respiration rates for soils incubated at

15–25 8C tended to be greatest under wetter conditions at

all three sites, with differences for the pinyon canopies most

pronounced (Fig. 2a – c). Soil respiration tended to

increase with increase in soil moisture for all soil types.

Differences in soil respiration rates between different

moistures were significant, ðP , 0:05Þ more consistently

for soils incubated under warmer temperatures, though the

wettest soils (20.03 and 20.05 MPa) usually had higher

respiration rates than the drier (21.00 and 21.50 MPa)

soils (Fig. 2a–c).

Fig. 2. Soil respiration for soils from the pinyon–juniper (PJ) site incubated under four temperatures and four soil moisture contents. Different lower case letters

indicate significant ðP , 0:05Þ differences between samples incubated under similar temperatures but different soil moisture contents. Different capital letter

indicate significant ðP , 0:05Þ differences between samples incubated under similar soil moistures, but different temperatures.

R.T. Conant et al. / Soil Biology & Biochemistry 36 (2004) 945–951948

Trends observed at the PP site were similar to those at the

PJ site (Fig. 3). Soil respiration tended to be greatest for

soils incubated at 25 8C, though differences were significant

ðP , 0:05Þ for canopy soils only for the driest soils (Fig. 3b).

Soils incubated at 5 8C had significantly ðP , 0:05Þ lower

respiration rates than soils incubated at 15 8C (Fig. 3).

Similar to the other sites, soil respiration tended to increase

with soil water potential; rates were always significantly

ðP , 0:05Þ greater under the wettest soil moisture

conditions (20.03 MPa), and usually under the next wettest

(20.05 MPa), than the two driest incubation moisture

conditions (21.00 and 21.50 MPa).

Soil respiration quotients (Q10 values) were always

significantly ðP , 0:05Þ greater for the wettest soils than for

the driest soils (Table 3). For the DS and PJ-interspace soils,

Fig. 3. Soil respiration for soils from the PP site incubated under four temperatures and four soil moisture contents. Different lower case letters indicate

significant ðP , 0:05Þ differences between samples incubated under similar temperatures but different soil moisture contents. Different capital letter indicate

significant ðP , 0:05Þ differences between samples incubated under similar soil moistures, but different temperatures.

Table 3

Soil respiration quotients ðQ10) for soils incubated at four water potentials

Site Cover type Water potential (MPa)

20.03 20.50 21.00 21.50

DS Interspace 2.78 (a) 1.95 (b) 1.61 (bc) 1.56 (c)

PJ Interspace 2.90 (a) 2.67 (a) 2.66 (a) 2.28 (b)

PJ Juniper canopy 4.32 (a) 4.52 (a) 2.68 (b) 2.52 (b)

PJ Pinyon canopy 2.84 (a) 3.48 (ab) 3.89 (b) 1.66 (c)

PP Interspace 3.16 (a) 2.01 (b) 2.03 (b) 2.01 (b)

PP Ponderosa pine canopy 3.17 (a) 3.19 (a) 3.26 (a) 2.30 (b)

Different letters indicate significant differences ðP , 0:05Þ in Q10

values between different water potentials.

R.T. Conant et al. / Soil Biology & Biochemistry 36 (2004) 945–951 949

Q10 values decreased with decrease in soil moisture.

The highest Q10 values for the pinyon and juniper

canopy soils at the PJ site and the ponderosa canopy at

the PP site were observed under dried conditions (20.50,

21.00, and 21.00, respectively). Q10 values averaged

across all soils decreased with soil moisture, ranging

from 3.15 (at 20.03 MPa) to 2.06 (at 21.5 MPa).

Averaged across all moisture contents, Q10s at the DS site

were lowest (1.97), and the interspace (2.80 and 2.31 for

PJ-interspace and PP-interspace, respectively) soils were

lower than the canopy soils at the other two sites (3.51, 2.99,

and 2.98 for PJ-juniper, PJ-pinyon, and PP-ponderosa,

respectively).

SI respiration rates increased with temperature for all

four different soils (Fig. 4). SI respiration rates were

significantly greater for the PP-ponderosa canopy soils than

for the other three soils at six of the eight incubation

temperatures; differences between all other soils at all

temperatures were insignificant (Fig. 4). Soil respiration

quotients were similar for all soils, ranging from 2.2

(PP-interspace) to 2.8 (PJ-interspace). Compared to Q10s

calculated from soil respiration rates for bulk soils, SIR Q10s

were similar for the DS-interspace and PJ-interspace

soils, but were considerably lower than those for the

PP-interspace and PP-ponderosa canopy soils.

4. Discussion

Results from this work support the hypothesis—derived

from in situ field measurements (Conant et al., 1998) and

experimental manipulations (Conant et al., 2001)—that soil

respiration responses to increases in temperature are

ameliorated at low soil moisture content. At low soil

moisture content soil respiration was positively related to

temperature for all soils, but responses were significantly

smaller. Field studies in other locations have shown similar

responses to increases in temperature under dry conditions,

but interpreting those results is complicated since

temperature increases dry out the soil (Davidson et al.,

1998). Likewise, a number of soil warming experiments

have concluded that decreases in soil moisture concomitant

with increases in temperature is a likely explanation for

limited positive responses of soil respiration to increased

temperature (e.g. Rustad et al., 2001). Our results

demonstrate that soil respiration responses to increases in

temperature are constrained by soil moisture for soils with a

range of litter quality, soil textures, and microbial

communities.

Soil respiration quotients from these incubations, ranging

from 1.3 to 5.1, fall within the range of those studies

reported elsewhere (Kirschbaum, 1995). Whereas other

studies investigating soil respiration in laboratory

incubations without water limitations have demonstrated a

negative relationship between mean incubation temperature

and Q10 response (Kirschbaum, 1995), our data follow the

opposite trend. Q10 values at lower temperatures (5–15 or

15–25 8C for the DS soil) tended to be greater than those for

warmer incubation temperatures; differences were smaller

under dried incubation conditions. SI respiration Q10 values,

however, did tend to decrease with increase in incubation

temperature. Lack of agreement between these data suggests

that decomposition of soil organic matter, which is more

recalcitrant than the added substrate, requires overcoming

higher activation energy.

It is interesting to note that, with the exception of the DS

site, Q10s averaged across all incubation moistures differed

little between sites. We expected that poor litter quality at

the higher elevation sites would lead to smaller differences

in respiration rates between different temperatures and, thus,

lower Q10s. Bulk soil respiration independent of soil C

(not shown) was lowest for the DS-interspace and PJ-inter-

space soils under all conditions indicating that these soils

contain less easily decomposable material, suggesting that

respiration responses to temperature may have been limited

by soil C content. Gallardo and Schesinger (1992)

demonstrated that in Chihuahuan desert soils as the ratio

of C:N decreased, microbial biomass became limited by C,

which may have been the case for the DS-interspace and

PJ-interspace soils. Conversely, larger responses for the

PJ-canopy and PP soils suggest that soil respiration in these

soils is not C limited.

This research clearly demonstrates that soil respiration

responses to changes in temperature will be a function of

direct impacts on the activity of decomposers. Furthermore,

these short-term responses will be impacted by soil moisture

and microbial community characteristics and can be altered

by soil C quality. Over the longer-term shifts in microbial

community composition, changes in the amount, timing,

and quality of litter inputs, and ultimately different soil C

quality may drive changes in soil C formation and turnover.

However, the results reported here corroborate field-based

observations that soil respiration responses to increase in

temperature appear to be constrained by low soil moisture.

Fig. 4. Soil respiration rates for four soils incubated at eight temperatures.

R.T. Conant et al. / Soil Biology & Biochemistry 36 (2004) 945–951950

Our results provide support for modeling approaches that

use multiplicative temperature and moisture decomposition

rate reducing functions (e.g. Parton et al., 1987) and have

important implications for understanding global change

impacts on C cycling since moisture stress/limitations occur

across such a large portion of terrestrial ecosystems.

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